|Year : 2013 | Volume
| Issue : 2 | Page : 44-49
Can the reduced level of alveolar bone in the initial stages of juvenile periodontitis anterior to the first molar be explained as arrest in alveolar bone growth?
Department of Orthodontics, Institute of Odontology, Faculty of Health Sciences, University of Copenhagen, Copenhagen N, Denmark
|Date of Web Publication||5-Jun-2013|
Department of Orthodontics, Institute of Odontology, Faculty of Health Sciences, University of Copenhagen, 20 Nørre Allé, DK-2200 Copenhagen N
Source of Support: The IMK foundation is acknowledged for financial support., Conflict of Interest: None
Introduction : It is generally agreed that juvenile periodontitis is more likely caused by genetic factors than environmental/bacterial factors. Until now, all research reports focus on alveolar bone destruction as a characteristic symptom. This is questioned in the present study. The Hypothesis : It is hypothesized that initial so-called bone loss in juvenile periodontitis can be explained as arrest in alveolar bone apposition during alveolar growth. Therefore, the purposes of this study are to analyze the morphology of cortical bone at the alveolar process located between the second premolar and first molar and to analyze whether the time of occurrence of juvenile periodontitis coincides with the time of the body growth spurt maximum of the individual. Orthopantomograms and dental films from 29 patients diagnosed with juvenile periodontitis were analyzed. Visual assessment of cortical bone on the alveolar process anterior to the first molar was performed. In addition, skeletal hand maturation was scored on hand radiographs from five patients and the maturity was related to body height. The results showed that in 18 patients the alveolar bone had a distinct compact with a normal level compared to the enamel cementum border of the second premolar and a pathological deep level compared to the enamel cementum border of the first molar. This abnormal alveolar bone level was first diagnosed shortly after pubertal maximum. Furthermore, 11 patients had uneven, indistinct alveolar cortical bone with the same abnormal level compared to the column of the second premolar and first molar. Evaluation of the Hypothesis: As a conclusion, it is evaluated that patients in the early stage of juvenile periodontitis have a bone loss due to arrest in alveolar bone growth anterior to the first molars during the early stage of the disease. Thereafter, the destruction of the cortical bone occurs.
Keywords: Alveolar bone, eruption, growth, juvenile periodontitis, resorption
|How to cite this article:|
Kjaer I. Can the reduced level of alveolar bone in the initial stages of juvenile periodontitis anterior to the first molar be explained as arrest in alveolar bone growth?. Dent Hypotheses 2013;4:44-9
|How to cite this URL:|
Kjaer I. Can the reduced level of alveolar bone in the initial stages of juvenile periodontitis anterior to the first molar be explained as arrest in alveolar bone growth?. Dent Hypotheses [serial online] 2013 [cited 2021 Jan 21];4:44-9. Available from: http://www.dentalhypotheses.com/text.asp?2013/4/2/44/113007
| Introduction|| |
It is generally agreed that juvenile periodontitis is more likely caused by genetic factors than environmental/bacterial factors. Until now, all research reports focus on alveolar bone destruction as a characteristic symptom. This is questioned in the present study, which suggests that the localized "bone destruction" is not destruction but lack of alveolar bone apposition during pubertal growth.
It is characteristic of juvenile periodontitis that the disease in its initial stages appears in well-defined regions in the dental arches. These regions are located between the second premolar and the first molar and in the incisor regions.  These are the same regions, in which agenesis is most frequently observed.  Juvenile periodontitis and agenesis are both hereditary conditions. ,, The question is thus why these regions are especially exposed to juvenile periodontitis and agenesis. In this connection, the innervation has previously been in focus as a possible factor of importance.  Previous studies have shown that the innervation is necessary for dental formation , and for dental eruption.  With eruption follows alveolar bone growth, but specific information on how the alveolar bone growth is initiated is still lacking. It has been shown that osteoblasts have neuroreceptors  and positivity of protein gene product, marking neurofibrils have also been demonstrated immunohistochemically in prenatal alveolar bone cells. 
Mapping of the jaw innervation has shown that there is a change in the innervation path between the second premolar and the first molar in both maxilla and mandible [Figure 1].  Similar changes are seen between the central incisors and between maxillary lateral incisors and canines [Figure 1]. Thus, a pattern in the innervation exists, which corresponds to the pattern registered in initial sites of juvenile periodontitis and to the pattern in the most common types of agenesis. This pattern reflects not only the pattern of innervation, but also the pattern of neural crest cell migration.  Growth studies by Björk with metal markers inserted into the jaws showed that continued tooth eruption and growth at the surrounding alveolar process takes place in childhood and youth.  Björk and co-workers also showed that the growth quantity varied during childhood and youth, being more extensive during puberty [Figure 2]. , Furthermore, in the incisor region this puberty growth spurt has been documented in tooth eruption and alveolar bone apposition [Figure 2].  How tooth eruption is coordinated with and followed by growth of the surrounding alveolar bone is not known.
|Figure 1: Schematic drawing of the jaw/tooth innervation on an orthopantomogram from an adult. Note that there are specific main nerve paths in both jaws for the incisors, the canines/premolars and the molars. The colors in the different jaw segments follow the innervation path and indicate different mesenchymal origins from the neural crest. The predilection sites for juvenile periodontitis are in the region between the colored segments|
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|Figure 2: Schematic drawings of central incisor eruption, left, and also first molar eruption, right, in maxillae from two patients with the metal implants for superimposing of radiographs. The ages of the radiographs are indicated in years and months. Note that incisors as well as first molars have an "eruption spurt" during puberty. Reproduced from articles by Siersbæk- Nielsen, left, and Skieller, right|
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In cases of juvenile periodontitis, it can be hypothesized that the alveolar bone growth with intensive deposits of bony tissue during the pubertal growth spurt does not take place in certain regions. These are regions between the second premolar and the first molar and regions located distally to the laterals in the upper jaw and mesially to the incisors in both jaws. The question is what is common for these regions where bone apposition fails.
| The Hypothesis|| |
The hypothesis in this study is that in the initial stages of juvenile periodontitis, normal continued eruption takes place of all teeth, but that the osseous growth of the alveolar process does not as normally follow eruption in the border regions between innervation paths. Thus, the failure in alveolar bone apposition is manifested as osseous posches resembling osseous destruction after infection and resorption.
Evidence supporting the hypothesis
The purpose of this work is to prove the hypothesis by:
- Analyzing the bone level according to the enamel cementum junction in the first molar/second premolar regions.
- Analyzing whether the time of occurrence of juvenile periodontitis coincides with the time of the height maximum of the individual or to the period immediately after.
| Materials and Methods|| |
Radiographic material from 29 young individuals was included in this study. The material comprised panoramic radiographs from 29 individuals and dental films from 27 of these. The radiographic material was forwarded from municipal dental clinics in Denmark by written request. The radiographs requested were the first radiographs taken after juvenile periodontitis had been diagnosed.
Furthermore, available hand radiographs were requested from the age when juvenile periodontitis was first diagnosed. Hand radiographs including height measurements were available from five patients. This material had been obtained in connection with orthodontic treatment planning.
Contour of alveolar bone deficit
A visual assessment was performed of bone level according to the enamel cementum junction. Bone contour, particularly of the cortical lamina, at the location of initial bone deficit at the alveolar process was analyzed.
The individual growth activity was estimated based on body height measurements and bone maturity evaluated on hand radiographs after methods by Greulich and Pyle  and Tanner et al. 
| Results|| |
With regards to osseous structure, two different patterns of bone morphology and bone level appeared.
Eighteen patients had an alveolar bony contour characterized by a distinct compact a bone without resorptive changes [Figure 3] and [Figure 4]. There were no clear signs of resorptive processes. It was characteristic that the bony contour appeared oblique, compared to the enamel cementum borderlines of the first molar and second premolar. The bone level was normal distally to the second premolar and abnormally low mesially to the first molar [Figure 3] and [Figure 4]. This appearance was considered to be the characteristic morphology of the initial sides of juvenile periodontitis.
|Figure 3: Dental film from a girl aged 14 (group 1 patient) with oblique alveolar bone level mesially to the left upper first molar. Other bone levels are normal. In the inserted diagram, the arrow indicates the borderline areas between jaw segments innervated differently|
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|Figure 4: A dental film from a boy aged 15 (group 1 patient) showing oblique alveolar bone contours mesially to the left upper and lower first molars. Other bone levels are normal. In the inserted diagram the arrow indicates the borderline areas between jaw segments innervated differently|
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Furthermore, 11 patients had uneven, indistinct alveolar cortical bone with the same abnormal level compared to the column of the second premolar and first molar [Figure 5]. The condition was not strictly located to the characteristic initial sites of juvenile periodontitis [Figure 5].
|Figure 5: Two dental films from two girls (aged 15, upper, and 12, lower). The alveolar bone levels are generally low. Group 2 patients. The patients may have been group 1 patients prior to infection and resorption|
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As a conclusion, it is hypothesized that patients diagnosed with juvenile periodontitis have arrest in alveolar bone growth during the early stage of the disease. Thereafter, the destruction of the cortical bone occurs.
Relation to pubertal growth spurt
In the five patients with information on the general body growth and body maturity, the age when juvenile periodontitis was diagnosed corresponded to ½-1½ years after pubertal growth maximum [Figure 6]. As the alveolar bone growth is associated with growth in general body height, this information supports the hypothesis.
|Figure 6: The two curves to the left indicate the body height (upper) and the growth velocity (lower) expressed as yearly increments in height for girls. The black dots mark a girl aged 12 years 11 month. The girl, recently diagnosed with juvenile periodontitis, is a few centimeters higher than the average for her age (upper curve) and she has passed her pubertal maximum (lower curve). The inserted schematic drawing of a first molar and its surrounding alveolar bone indicates that the continued eruption from first emergence at about 6 years of age to arrested body growth is associated with variations in annual bone apposition. The longest distance between two black lines marking the top of the alveolar bone at different ages between 6 and 17 years indicates the pubertal maximum. To the right the hand radiograph from the girl with a maturity stage according to Greulich and Pyle of the middle phalanx of the third finger: The epiphysis caps its diaphysis (MP3cap). This maturity stage corresponds to about 9 months after pubertal maximum|
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| Evaluation of the Hypothesis|| |
The localization of the initial areas of lack of bone characteristic in juvenile periodontitis, correspond to the normal locations of tooth agenesis. It is hypothesized that this concurrency is associated with the pattern of jaw innervation.
In the periodontal literature, there are extensive and thorough studies on prevalence and types of periodontal diseases in childhood and adolescence. Classification and diagnostic characteristics of these diseases have been in focus for the recommendation of therapeutic management.  Furthermore, the risk factors for periodontitis in children and adolescents have been investigated extensively.  The results of the present study indicate that the initial osseous defects in exposed regions of the alveolar process in patients with juvenile periodontitis are in the initial stage not resorption defects caused by an infection, but regions where the natural and under normal conditions intensive growth of the alveolar process fails during puberty. The condition is a result of arrest in growth of the alveolar process, associated with normal eruption of teeth. Incisors and first molars are the teeth that erupt early (about 6 years of age) and where periodontal adaption and remodeling, therefore, are required from early childhood. It is interesting that neither the precise tissue interaction resulting in the dental eruption, nor the tissue interaction between the tooth and its surrounding alveolar bone taking place during eruption, are known.
It is obvious that innervation plays a role both in the eruption process and in the alveolar bone growth. ,, It is also well-known that mumps virus can spread along the peripheral nerves resulting in arrested eruption.  With regards to the ongoing changes of the periodontium during eruption, there is not much exact knowledge.
In connection with registration of the initial osseous changes in juvenile periodontitis, the question is when and why infectious changes occur. A suggestion could be that infection begins secondarily to the osseous posches, which may explain the visual difference in the cortical bone observed in the study. The suggestion is still hypothetical.
It is interesting in this connection that the tooth and its surrounding alveolar bone apparently can alter dependently, e.g., in cases where both arrested eruption and arrested growth of the alveolar process are observed, and independently.  The independent alteration is seen in cases where a tooth is arrested in eruption, but where the alveolar bone continues its growth and gradually covers the tooth arrested in eruption or when the tooth erupts normally, but without concomitant growth of the alveolar bone [Figure 7]. In the case of juvenile periodontitis (group 1), it is presumably the tooth, which moves in the occlusal direction and the growth of the alveolar process mesially to the first molar that is arrested in bone apposition.
In conclusion, this study indicates the necessity of considering the different developmental fields from the neural crest of the jaws.  In the etiological explanation of diseases and changes in craniofacial and dental development, the fields and specifically the borders between these regional developmental fields are particularly exposed.
|Figure 7: Drawings indicating eruption of the lower first molar and growth of its surrounding alveolar bone. Left: Normal annual increment of alveolar bone apposition as indicated with black lines to the right. Eruption and bone apposition are coordinated as under normal conditions. Same figure as illustrated in Figure 6. Right: These two drawings indicate abnormal coordination of eruption and alveolar bone apposition. To the left the bone has not been laid down mesially to the molar during eruption (group 1 in the present study). To the right eruption is arrested by ankylosis while alveolar bone has continued normal yearly growth deposits|
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By inserting metal markers in the jaws, it was documented that the intensity of alveolar bone growth in children varies during different growth periods. ,, Thus, the amount of bone laid down on the alveolar process is less during the stage of pubertal minimum than in the stage of pubertal maximum also named the period of pubertal growth spurt. This knowledge is important for understanding why failure in alveolar bone apposition appears at the age of puberty.
A schematic diagram of the postnatal jaw innervation is illustrated in [Figure 1]. From this illustration, it is clear that initial "bone deficit" in juvenile periodontitis occurs where the course of the nerve branches changes. The nerve pattern also expresses the different segments constituting the jaw. It is well-known that the jaws are formed early by neural crest cells migrating from the crest of the neural tube from different areas to different the jaw segments. The places of predilection for juvenile periodontitis are not just border areas between innervation, but between jaw parts formed from different areas from the neural crest.
The different regions in the jaws originating from different areas of the neural crest allow us to understand patterns of dental deviations that have not been understood before.  The pattern of agenesis, not caused primarily by failure in the ectoderm, is characterized by the absence of second premolars, upper laterals and lower centrals.  This pattern seems to be identical to the pattern of "bone deficit" in juvenile periodontitis and is explained by a deviant innervation as part of a regional border symptom. The heredity of juvenile periodontitis and that of agenesis may be associated with the genetic influence on the neural crest cell migration and of the innervation fields in the jaws.
Conclusively, this work indicates that innervation of the periodontal membrane  may be an important factor in the development of juvenile periodontitis. What this means for the treatment of juvenile periodontitis is an aspect to be considered in future studies. Furthermore, the different patterns in craniofacial growth, , which are associated with different patterns of alveolar bone apposition may be considered further. ,
| Acknowledgments|| |
Dentists and specialists in orthodontics in Denmark are acknowledged for forwarding radiographs to the present study. The IMK Foundation is acknowledged for funding. Maria Kvetny, MA, is acknowledged for linguistic support and manuscript preparation.
| References|| |
|1.||Hørmand J, Frandsen A. Juvenile periodontitis. Localization of bone loss in relation to age, sex, and teeth. J Clin Periodontol 1979;6:407-16. |
|2.||Rølling S. Hypodontia of permanent teeth in Danish schoolchildren. Scand J Dent Res 1980;88:365-9. |
|3.||Kilian M, Frandsen EV, Haubek D, Poulsen K. The etiology of periodontal disease revisited by population genetic analysis. Periodontol 2000 2006;42:158-79. |
|4.||Michalowicz BS. Genetic and heritable risk factors in periodontal disease. J Periodontol 1994;65 Suppl 5:479-88. |
|5.||Stockton DW, Das P, Goldenberg M, D'Souza RN, Patel PI. Mutation of PAX9 is associated with oligodontia. Nat Genet 2000;24:18-9. |
|6.||Kjaer I. Can the location of tooth agenesis and the location of initial bone loss seen in juvenile periodontitis be explained by neural developmental fields in the jaws? Acta Odontol Scand 1997;55:70-2. |
|7.||Kjaer I, Kocsis G, Nodal M, Christensen LR. Aetiological aspects of mandibular tooth agenesis - Focusing on the role of nerve, oral mucosa, and supporting tissues. Eur J Orthod 1994;16:371-5. |
|8.||Becktor KB, Hansen BF, Nolting D, Kjaer I. Spatiotemporal expression of NGFR during pre-natal human tooth development. Orthod Craniofac Res 2002;5:85-9. |
|9.||Parner ET, Heidmann JM, Kjaer I, Vaeth M, Poulsen S. Biological interpretation of the correlation of emergence times of permanent teeth. J Dent Res 2002;81:451-4. |
|10.||Lerner UH. Neuropeptidergic regulation of bone resorption and bone formation. J Musculoskelet Neuronal Interact 2002;2:440-7. |
|11.||Kjaer I, Nolting D. Immunohistochemical PGP 9.5 positivity in human osteoblasts may indicate that compensatory and dysplastic craniofacial growth are under control by peripheral nerves. Orthod Craniofac Res 2008;11:196-200. |
|12.||Kjaer I. Neuro-osteology. Crit Rev Oral Biol Med 1998;9:224-44. |
|13.||Bjork A. Sutural growth of the upper face studied by the implant method. Rep Congr Eur Orthod Soc 1964;40:49-65. |
|14.||Skieller V. Growth stimulation of the upper face in a case of mesial occlusion analyzed by the implant method. Tandlaegebladet 1971;75:1296-306. |
|15.||Iseri H, Solow B. Continued eruption of maxillary incisors and first molars in girls from 9 to 25 years, studied by the implant method. Eur J Orthod 1996;18:245-56. |
|16.||Siersbaek-Nielsen S. Rate of eruption of central incisors at puberty: An implant study on eight boys. Tandlaegebladet 1971;75:1288-95. |
|17.||Greulich WW, Pyle SI. Radiographic atlas of skeletal development of the hand and wrist. Stanford: Stanford University Press; 1950. |
|18.||Tanner JM, Whitehouse RH, Healy MJ. A new system for estimating skeletal maturity from the hand and wrist, with standards derived from a study of 2.600 healthy British children, Part II: The scoring system. Paris: International Children's Centre; 1962. |
|19.||Oh TJ, Eber R, Wang HL. Periodontal diseases in the child and adolescent. J Clin Periodontol 2002;29:400-10. |
|20.||Albandar JM, Rams TE. Risk factors for periodontitis in children and young persons. Periodontol 2000 2002;29:207-22. |
|21.||Bang E, Kjaer I, Christensen LR. Etiologic aspects and orthodontic treatment of unilateral localized arrested tooth-development combined with hearing loss. Am J Orthod Dentofacial Orthop 1995;108:154-61. |
|22.||Nielsen SH, Becktor KB, Kjaer I. Primary retention of first permanent mandibular molars in 29 subjects. Eur J Orthod 2006;28:529-34. |
|23.||Kjaer I. New diagnostics of the dentition on panoramic radiographs-focusing on the peripheral nervous system as an important aetiological factor behind dental anomalies. Orthod Waves 2012;71:1-16. |
|24.||Kjaer I, Nolting D. The human periodontal membrane: Focusing on the spatial interrelation between the epithelial layer of Malassez, fibers, and innervation. Acta Odontol Scand 2009;67:134-8. |
|25.||Björk A. The relationship of the jaws to the cranium. In: Lundstrøm A, editor. Introduction to Orthodontics. New York: McGraw-Hill; 1960. p. 104-40. |
|26.||Skieller V, Björk A, Linde-Hansen T. Prediction of mandibular growth rotation evaluated from a longitudinal implant sample. Am J Orthod 1984;86:359-70. |
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